Root tragedy of the commons: Revisiting the mechanisms of a misunderstood theory.

Fine root density in the soil is a plant functional trait of paramount importance for plant ecology and agriculture. Fine root proliferation by plants involves complex plant strategies that may depend on various abiotic and biotic factors. Concretely, the root tragedy of the commons (RToC) is a behavioral strategy predicted by game theory models in which interacting plants forage for soil resources inefficiently. Generally, researchers assume that the RToC is a proactive competition strategy directly induced by the non-self roots. In this opinion, I recall Hardin's original definition of the tragedy of the commons to challenge this notion. I argue that the RToC is a suboptimal phenotypically plastic response of the plants based on the soil resource information exclusively, and I discuss how this alternative perspective carries important implications for the design of experiments investigating the physiological mechanisms underlying observable plant root responses.

Future paths for the 'exploitative segregation of plant roots' model.

The exploitative segregation of plant roots (ESPR) is a theory that uses a game-theoretical model to predict plant root foraging behavior in space. The original model returns the optimal root distribution assuming exploitative competition between a pair of identical plants in soils with homogeneous resource dynamics. In this short communication, we explore avenues to develop this model further. We discuss: (i) the response of single plants to soil heterogeneity; (ii) the variability of the plant response under uneven competition scenarios; (iii) the importance of accounting for the constraints and limitations to root growth that may be imposed from the plant shoot; (iv) the importance of root functional traits to predict root foraging behavior; (v) potential model extensions to investigate facilitation by incorporating facilitative traits to roots, and (vi) the possibility of allowing plants to tune their response by accounting for non-self and non-kin root recognition. For each case, we introduce the topic briefly and present possible ways to encode those ingredients in the mathematical equations of the ESPR model, providing preliminary results when possible.

The exploitative segregation of plant roots.

Plant roots determine carbon uptake, survivorship, and agricultural yield and represent a large proportion of the world's vegetation carbon pool. Study of belowground competition, unlike aboveground shoot competition, is hampered by our inability to observe roots. We developed a consumer-resource model based in game theory that predicts the root density spatial distribution of individual plants and tested the model predictions in a greenhouse experiment. Plants in the experiment reacted to neighbors as predicted by the model's evolutionary stable equilibrium, by both overinvesting in nearby roots and reducing their root foraging range. We thereby provide a theoretical foundation for belowground allocation of carbon by vegetation that reconciles seemingly contradictory experimental results such as root segregation and the tragedy of the commons in plant roots.

Long-term simulated nitrogen deposition alters the plant cover dynamics of a Mediterranean rosemary shrubland in Central Spain through defoliation.

Nitrogen (N) deposition due to anthropogenic pollution is a major driver of the global biodiversity loss. We studied the effect of experimental N and phosphorus (P) fertilization (0, 10, 20, and 50 kg N ha-1 year-1 and 14 kg P ha-1 year-1 over the background deposition levels) on plant cover dynamics of a rosemary (Rosmarinus officinalis L.) shrubland after 8 years of nutrient addition in a semiarid Mediterranean ecosystem from Central Spain. We specifically aimed at testing whether N deposition has the potential to influence the observed expanding trend of woody vegetation into areas dominated by grassland, biological soil crusts, and bare soil. Our results show that N addition loads above 10 kg N ha-1 year-1 reverted the cover dynamics of shrubs. Under N addition conditions, N was no longer a limiting nutrient and other elements, especially P and calcium, determined the seasonal growth of young twigs. Interestingly, N fertilization did not inhibit the growth of young shoots; our estimates point to a reduced rosemary leaf lifespan that is driving individuals to death. This may be triggered by long-term accumulation of N compounds in leaves, suggesting the need to consider the old organs and tissues in long-lived perennial plants, where N toxicity effects could be more mediated by accumulation processes. Shrublands are a widely distributed ecosystem type in biodiverse Mediterranean landscapes, where shrubs play a key role as nurse plants. Therefore, the disappearance of shrublands may accelerate the biodiversity loss associated with other global change drivers, hamper the recruitment of seedlings of woody species, and, as a consequence, accelerate desertification.